The beauty and genius of a work of art may be reconceived, though its first material expression be destroyed; a vanished harmony may yet again inspire the composer; but when the last individual of a race of living beings breathes no more, another heaven and another earth must pass before such a one can be again.

~ William Beebe (1877–1962)

Once the most abundant bird in the world, with a population estimated to number somewhere between 3 and 5 billion in the early and mid-1800s, the sudden extinction of the passenger pigeon, Ectopistes migratorius, in 1914, raises the question of how such an abundant species could have become extinct in less than 50 years. A newly published study combines high throughput DNA technologies, ecological niche modelling and reconstructions of annual production of acorns upon which the birds fed to show that the passenger pigeon was not always super-abundant. Instead, this bird was an “outbreak” species that experienced dramatic population fluctuations in response to variations in annual acorn production. Thus, the extinction of the passenger pigeon likely was due to the combined effects of natural population fluctuations and human over-exploitation.

It was one of those career-altering dinner table discussions that seemed to carry on long into the night.

“We were talking about how evil humans can be to wildlife”, writes Hung Chih-Ming in email. As he recalled, most of his co-authors — Shou-Hsien Li, Bob Zink and others — were at that table when one of them mentioned the tragic story of the passenger pigeon, Ectopistes migratorius. These legendary North American birds were so numerous that their flocks blocked the sun from view for days in the early and mid-1800s; yet less than 50 years later, these birds — all of them — were gone forever.

“The passenger pigeon was once the most abundant bird in the world, and suddenly it disappeared totally from the Earth.”

Mind-boggling.

Passenger Pigeon skeleton. (Public domain.)

How could this be possible? Why did these birds disappear? Was this extinction due solely the murderous efficiency of gun-toting humans, or were there other, underlying factors that contributed to the demise of this species?

These are more interesting questions than they may appear to be at first glance. On one hand, it’s obvious that rare species with small geographic distributions are more likely to go extinct than are abundant, widespread species. But on the other hand, the loss of the passenger pigeon, especially with their vast numbers, had clearly defied all logic. Perhaps there was something special happening to these super-abundant and widespread birds that made them especially vulnerable to extinction? Would it be possible for the researchers identify what that could have been?

The questions fluttered through the gathering gloom like moths around a bright light. Before long, idle curiosity coalesced into a firm resolve, and the researchers, some still graduate students, others seasoned investigators, realised they’d established a team with one objective: to shed light on this mystery.

“[W]e realized 2014 would be the 100th anniversary of its extinction, so we started to plan this project.”

This project was initiated when Hung Chih-Ming was writing up his doctoral research under the supervision of Robert Zink, a professor of avian evolution at the University of Minnesota. Dr Hung is now a postdoctoral fellow in the lab of Shou-Hsien Li, a professor of Life Sciences at the National Taiwan Normal University.

The team concentrated on a few basic questions that they’d agreed would clarify some important details about the passenger pigeon’s murky life history; details that might help explain how humans could drive them to extinction.

Was the passenger pigeon always super-abundant?

To gain a clearer understanding of the ecology and evolution of the passenger pigeon, Dr Hung and his colleagues extracted DNA from nine tissue samples scraped from the toepads of specimens held in two museums, the Bell Museum of Natural History in Minneapolis and American Museum of Natural History in New York City. Because this DNA was quite old (known as ancient DNA or “aDNA”), the extraction process was challenging and required the researchers to develop special techniques (doi:10.1371/journal.pone.0056301). Even still, only three specimens provided useful aDNA.

The researchers sequenced the aDNA using high-throughput technologies and managed to piece together high-quality genomic sequences for the passenger pigeon — the longest genome sequence with the highest quality ever obtained for an extinct bird.

Co-author Pen-Jen Shaner, an assistant professor in the the department of Life Sciences at the National Taiwan Normal University, and her colleagues, Wei-Chung Liu and Te-Chin Chu, used two different mathematical approaches to estimate the passenger pigeon’s genetically effective population size (Ne). The genetically effective population size is an estimate of the total genetic variation found within a given population (doi:10.1017/S0016672300034455). Increased genetic variation is associated with a greater capacity to survive challenging circumstances. Genetic variation arises through mutation and recombination, whilst natural selection removes variation from a population.

Since the passenger pigeon’s census numbers were between 3 and 5 billion individuals in the mid-1800s, the researchers were surprised when they discovered that the passenger pigeon’s genetically effective population size (Ne) was remarkably small. The genetically effective population size, Ne, was just 3.3 × 10^5 (95% credible interval = 3.25–3.32 × 10^5), which is approximately 1/10,000 of the estimated number of individuals from the mid-1800s.

This small genetically effective population size suggests that passenger pigeons were not always super-abundant. Instead, their population changed by a thousand-fold over time, a situation seen under two circumstances. First, a low genetically effective population size is characteristic for species that experience wide population fluctuations that only occasionally number into the billions during an “outbreak” phase (doi:10.1017/S0016672300034455). For example, most people are familiar with several outbreak species, particularly lemmings, Lemmus lemmus, and snowshoe hares, Lepus americanus, in the Arctic, and Australian plague locusts, Chortoicetes terminifera.

But an alternative explanation for a low Ne is seen for species that historically had small numbers and only recently experienced a population explosion — a situation occurring in humans today.

To distinguish between the outbreak species and the population explosion hypotheses, the researchers tested the data using several models; genome-coalescent analysis, ecological niche models (models of climate) and models of carrying capacity. Genome-coalescent analysis calculates the time elapsed since individual passenger pigeon lineages diverged (Figure 2; larger view):

This model indicated that passenger pigeons experienced repeated rises and falls in population size, consistent with the “outbreak” species hypothesis.

Why did passenger pigeon populations fluctuate so dramatically?

Although passenger pigeons would eat a variety of foods, especially when breeding, they primarily were seed predators that specialised on acorns. Annual productions of acorns, chestnuts, and beechnuts — “mast” — varies tremendously on an annual basis and across the different tree species in North America. (For example, acorn production by red oaks, Quercus rubra, can vary as much as 12-fold between years, and for white oaks, Q. alba, as much as 136-fold.) Mast production is affected over large areas by inclement weather or by changes in population sizes of the seed predators that consume mast.

Acorns from small to large of the Willow Oak, Quercus phellos (very small, at center); the Southern Red Oak, Quercus falcata; the White Oak, Quercus alba; and the Scarlet Oak, Quercus coccinea; from southern Greenville County, SC, USA. (Credit: David Hill/CC BY 2.0.)

To estimate historic acorn production, Professor Shaner and her colleagues developed an ecological climate niche model. It was based upon fossil pollen records for northern and eastern North America and it inferred the oak coverage per square kilometre from 21,000 years before present up to the present day (Figure 4a; larger view). After calculating the historic oak cover, Professor Shaner and her colleagues calculated the passenger pigeon carrying capacity over this time period based on the average acorn production of red oaks (solid black dot; Figure 4b; larger view), and white oaks (open white dot; Figure 4b; larger view), collected from multiple sites and years, and their estimation that each pigeon consumed 30 acorns daily (Figure 4b; larger view):

What lessons can passenger pigeons teach us?

Taken together, the data from this study show that the passenger pigeon experienced large, natural population fluctuations — a surprise to the authors and to the reviewers of this paper, according to Dr Hung, since outbreak species have only ever been identified as either insects or rodents.

But other factors may have contributed significantly to the passenger pigeon’s population fluctuations — and ultimate demise. For example, the pigeons formed enormous roosting and breeding colonies that caused physical damage to trees (including mast trees) and to the surrounding areas. Of course, the large, highly social flocks and the close proximity of individual birds likely sped up transmission of infectious diseases, too. The birds’ natural behaviours may also have made them vulnerable to extinction for other reasons. For example, their conspicuous roosting and breeding behaviours could have made them an obvious target to predators (especially humans), which could have prevented recovery of their populations.

And speaking of humans, let us not forget that, in addition to uncontrolled hunting and ferocious habitat destruction, European immigrants may also have enhanced this bird’s last, final outbreak by unintentionally providing a supplemental food supply in the form of agricultural crops and by relieving hunting pressures by Native American indigenous peoples.

In this study, Dr Hung, Professor Shaner and their colleagues were not looking to discount or disregard the pivotal role that people played in the extinction of this bird. Instead, they were seeking to understand how humans could have reduced this seemingly endless population from billions to none in such a short time period. Based on their research findings, Dr Hung, Professor Shaner and their colleagues propose that the passenger pigeon’s population was already in a natural nosedive phase simultaneously with human over-exploitation in the late 1800s, and it was the combination of these two pressures that led to its sudden extinction.

But passenger pigeons can teach us other lessons too. For example, they are a tragic example that large, widespread populations may not be sufficient to protect a species from extinction — especially after people have focused their sights on the habitat or upon the animals themselves. Further, these iconic birds should remind us that we cannot accurately assess vulnerability to extinction without understanding each species’ special natural history.

Earliest published illustration of the passenger pigeon (a male), by Mark Catesby, 1731. (Plate 23 in Volume 1 of The Natural History of Carolina, Florida and Bahamas by Mark Catesby, George Edwards published in 1754. Also mentioned as Palumbus migratorius. Tree is red oak.) Public domain.